Epidermal growth factor upregulates serotonin transporter in human intestinal epithelial cells via transcriptional mechanisms

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 4, 2011, Pages

  Gill, Ravinder K ^a   Anbazhagan, Arivarasu Natarajan ^a   Esmaili, Ali ^a   Kumar, Anoop ^a   Nazir, Saad ^a   Malakooti, Jaleh ^a   Alrefai, Waddah A ^a   Saksena, Seema ^a  

^a JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

AP1; c jun; EGF; Serotonin transport; SERT

Indexed keywords

CIS ACTING ELEMENT; ELECTROLYTE; EPIDERMAL GROWTH FACTOR; MESSENGER RNA; N [4 (3 BROMOANILINO) 6 QUINAZOLINYL]ACRYLAMIDE; NUCLEAR PROTEIN; PROTEIN C FOS; PROTEIN C JUN; SEROTONIN; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CELL STRAIN CACO 2; CONTROLLED STUDY; ELECTROLYTE TRANSPORT; GENE; GENE DELETION; HSERTP1 GENE; HSERTP2 GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; NUTRIENT; PRIORITY JOURNAL; PROMOTER REGION; TRANSACTIVATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANALYSIS OF VARIANCE; CACO-2 CELLS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; UP-REGULATION;

EID: 79955058385     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00563.2010     Document Type: Article

References (49)

1. Alrefai WA, Annaba F, Sarwar Z, Dwivedi A, Saksena S, Singla A, Dudeja PK, Gill RK. Modulation of human Niemann-Pick C1-like 1 gene expression by sterol: role of sterol regulatory element binding protein 2. Am J Physiol Gastrointest Liver Physiol 292: G369-G376, 2007.
2. Banan A, Zhang LJ, Shaikh M, Fields JZ, Farhadi A, Keshavarzian A. Key role of PLC-gamma in EGF protection of epithelial barrier against iNOS upregulation and F-actin nitration and disassembly. Am J Physiol Cell Physiol 285: C977-C993, 2003.
3. Berger M, Gray JA, Roth BL. The expanded biology of serotonin. Annu Rev Med 60: 355-366, 2009.
4. Bishop WP, Wen JT. Regulation of Caco-2 cell proliferation by basolateral membrane epidermal growth factor receptors. Am J Physiol Gastrointest Liver Physiol 267: G892-G900, 1994.
5. Borthakur A, Gill RK, Tyagi S, Koutsouris A, Alrefai WA, Hecht GA, Ramaswamy K, Dudeja PK. The probiotic Lactobacillus acidophilus stimulates chloride/hydroxyl exchange activity in human intestinal epithelial cells. J Nutr 138: 1355-1359, 2008.
6. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
7. Carpenter G, Cohen S. Epidermal growth factor. J Biol Chem 265: 7709-7712, 1990.
8. Chen JJ, Li Z, Pan H, Murphy DL, Tamir H, Koepsell H, Gershon MD. Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: abnormal intestinal motility and the expression of cation transporters. J Neurosci 21: 6348-6361, 2001.
9. Coates MD, Johnson AC, Greenwood-Van Meerveld B, Mawe GM. Effects of serotonin transporter inhibition on gastrointestinal motility and colonic sensitivity in the mouse. Neurogastroenterol Motil 18: 464-471, 2006.
10. Coates MD, Mahoney CR, Linden DR, Sampson JE, Chen J, Blaszyk H, Crowell MD, Sharkey KA, Gershon MD, Mawe GM, Moses PL. Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 126: 1657-1664, 2004.
11. Donowitz M, Janecki A, Akhter S, Cavet ME, Sanchez F, Lamprecht G, Zizak M, Kwon WL, Khurana S, Yun CH, Tse CM. Short-term regulation of NHE3 by EGF and protein kinase C but not protein kinase A involves vesicle trafficking in epithelial cells and fibroblasts. Ann NY Acad Sci 915: 30-42, 2000.
12. Esmaili A, Nazir S, Singla A, Dudeja A, Saksena S, Raheja G, Alrefai WA, Gill RK. Epidermal growth factor (EGF) stimulates serotonin transporter function and expression via transcriptional mechanisms in human intestinal epithelial cells (Abstract). Gastroenterology 136, Suppl 1: A-567, 2009.
13. Esmaili A, Nazir SF, Borthakur A, Yu D, Turner JR, Saksena S, Singla A, Hecht GA, Alrefai WA, Gill RK. Enteropathogenic Escherichia coli infection inhibits intestinal serotonin transporter function and expression. Gastroenterology 137: 2074-2083, 2009.
14. Farrell RJ. Epidermal growth factor for ulcerative colitis. N Engl J Med 349: 395-397, 2003.
15. Faure C, Patey N, Gauthier C, Brooks EM, Mawe GM. Serotonin signaling is altered in irritable bowel syndrome with diarrhea but not in functional dyspepsia in pediatric age patients. Gastroenterology 139: 249-258, 2010.
16. Fisch TM, Prywes R, Roeder RG. An AP1-binding site in the c-fos gene can mediate induction by epidermal growth factor and 12-O-tetradecanoyl phorbol-13-acetate. Mol Cell Biol 9: 1327-1331, 1989.
17. Foley KF, Pantano C, Ciolino A, Mawe GM. IFN-gamma and TNFalpha decrease serotonin transporter function and expression in Caco2 cells. Am J Physiol Gastrointest Liver Physiol 292: G779-G784, 2007.
18. + exchange activity. Proc Soc Exp Biol Med 201: 289-295, 1992.
19. Gill RK, Borthakur A, Hodges K, Turner JR, Clayburgh DR, Saksena S, Zaheer A, Ramaswamy K, Hecht G, Dudeja PK. Mechanism underlying inhibition of intestinal apical Cl/OH exchange following infection with enteropathogenic E. coli. J Clin Invest 117: 428-437, 2007.
20. Gill RK, Pant N, Saksena S, Singla A, Nazir TM, Vohwinkel L, Turner JR, Goldstein J, Alrefai WA, Dudeja PK. Function, expression, and characterization of the serotonin transporter in the native human intestine. Am J Physiol Gastrointest Liver Physiol 294: G254-G262, 2008.
21. 4 receptors and activation of PKC alpha in human intestinal epithelial cells. Gastroenterology 128: 962-974, 2005.
22. Godley JM, Brand SJ. Regulation of the gastrin promoter by epidermal growth factor and neuropeptides. Proc Natl Acad Sci USA 86: 3036-3040, 1989.
23. Haub S, Ritze Y, Bergheim I, Pabst O, Gershon MD, Bischoff SC. Enhancement of intestinal inflammation in mice lacking interleukin 10 by deletion of the serotonin reuptake transporter. Neurogastroenterol Motil 22: 826-834, 2010.
24. Keely SJ, Barrett KE. ErbB2 and ErbB3 receptors mediate inhibition of calcium-dependent chloride secretion in colonic epithelial cells. J Biol Chem 274: 33449-33454, 1999.
25. Linden DR, White SL, Brooks EM, Mawe GM. Novel promoter and alternate transcription start site of the human serotonin reuptake transporter in intestinal mucosa. Neurogastroenterol Motil 21: 534-541, 2009.
26. + exchanger NHE3 promoter. Am J Physiol Gastrointest Liver Physiol 282: G491-G500, 2002.
27. Martel F. Recent advances on the importance of the serotonin transporter SERT in the rat intestine. Pharmacol Res 54: 73-76, 2006.
28. Martel F, Monteiro R, Lemos C. Uptake of serotonin at the apical and basolateral membranes of human intestinal epithelial (Caco-2) cells occurs through the neuronal serotonin transporter (SERT). J Pharmacol Exp Ther 306: 355-362, 2003.
29. McCole DF, Rogler G, Varki N, Barrett KE. Epidermal growth factor partially restores colonic ion transport responses in mouse models of chronic colitis. Gastroenterology 129: 591-608, 2005.
30. Menard D, Corriveau L, Arsenault P. Differential effects of epidermal growth factor and hydrocortisone in human fetal colon. J Pediatr Gastroenterol Nutr 10: 13-20, 1990.
31. Menard D, Pothier P. Radioautographic localization of epidermal growth factor receptors in human fetal gut. Gastroenterology 101: 640-649, 1991.
32. Merchant JL, Shiotani A, Mortensen ER, Shumaker DK, Abraczinskas DR. Epidermal growth factor stimulation of the human gastrin promoter requires Sp1. J Biol Chem 270: 6314-6319, 1995.
33. - secretion by EGF. Am J Physiol Cell Physiol 294: C1362-C1370, 2008.
34. Ren Y, Satoh T, Yamada M, Hashimoto K, Konaka S, Iwasaki T, Mori M. Stimulation of the preprothyrotropin-releasing hormone gene by epidermal growth factor. Endocrinology 139: 195-203, 1998.
35. Riegler M, Sedivy R, Sogukoglu T, Castagliuolo I, Pothoulakis C, Cosentini E, Bischof G, Hamilton G, Teleky B, Feil W, Lamont JT, Wenzl E. Epidermal growth factor attenuates Clostridium difficile toxin A-and B-induced damage of human colonic mucosa. Am J Physiol Gastrointest Liver Physiol 273: G1014-G1022, 1997.
36. Riegler M, Sedivy R, Sogukoglu T, Cosentini E, Bischof G, Teleky B, Feil W, Schiessel R, Hamilton G, Wenzl E. Effect of growth factors on epithelial restitution of human colonic mucosa in vitro. Scand J Gastroenterol 32: 925-932, 1997.
37. - exchange activity in Caco-2 cells by serotonin. J Biol Chem 280: 11859-11868, 2005.
38. Saksena S, Singla A, Goyal S, Katyal S, Bansal N, Gill RK, Alrefai WA, Ramaswamy K, Dudeja PK. Mechanisms of transcriptional modulation of the human anion exchanger SLC26A3 gene expression by IFNgamma. Am J Physiol Gastrointest Liver Physiol 298: G159-G166, 2010.
39. Schlessinger J. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell 110: 669-672, 2002.
40. Shaulian E. AP-1-the Jun proteins: oncogenes or tumor suppressors in disguise? Cell Signal 22: 894-899.
41. Sinha A, Nightingale J, West KP, Berlanga-Acosta J, Playford RJ. Epidermal growth factor enemas with oral mesalamine for mild-to-moderate left-sided ulcerative colitis or proctitis. N Engl J Med 349: 350-357, 2003.
42. Spiller R. Serotonin and GI clinical disorders. Neuropharmacology 55: 1072-1080, 2008.
43. Ulshen MH, Lyn-Cook LE, Raasch RH. Effects of intraluminal epidermal growth factor on mucosal proliferation in the small intestine of adult rats. Gastroenterology 91: 1134-1140, 1986.
44. - transport in T84 human colonic epithelial cells. Am J Physiol Cell Physiol 271: C914-C922, 1996.
45. i-IIb gene promoter by epidermal growth factor. Am J Physiol Cell Physiol 280: C628-C636, 2001.
46. Xu H, Collins JF, Bai L, Kiela PR, Lynch RM, Ghishan FK. Epidermal growth factor regulation of rat NHE2 gene expression. Am J Physiol Cell Physiol 281: C504-C513, 2001.
47. Xu H, Inouye M, Hines ER, Collins JF, Ghishan FK. Transcriptional regulation of the human NaPi-IIb cotransporter by EGF in Caco-2 cells involves c-myb. Am J Physiol Cell Physiol 284: C1262-C1271, 2003.
48. Xu H, Zhang B, Li J, Chen H, Tooley J, Ghishan FK. Epidermal growth factor inhibits intestinal NHE8 expression via reducing its basal transcription. Am J Physiol Cell Physiol 299: C51-C57, 2010.
49. Zheleznova NN, Wilson PD, Staruschenko A. Epidermal growth factor-mediated proliferation and sodium transport in normal and PKD epithelial cells. Biochim Biophys Acta (October 16, 2010). doi: 10.1016/j. bbadis.2010.10.004.